MARINE ECOLOGY PROGRESS SERIES Mar Ecol Prog Ser
Vol. 375: 41–52, 2009
doi: 10.3354/meps07735 Published January 27
INTRODUCTION
Eutrophication is a frequent and widespread pheno-menon associated with the human utilisation of coastal areas of oceans, and its development is generally de-scribed using ‘input-response’ models (Cloern 2001). These models assume that an increase in nutrient con-centrations causes an increase of primary production that, if surpassing certain threshold levels, primes detrimental effects on the ecosystem (Pinckney et al. 2001).
The trophic status of marine ecosystems is generally assessed through chemical measurements (e.g. inor-ganic nitrogen and phosphorus) and/or surrogate
mea-surements of algal biomass in the water column (Ste-fanou et al. 2000). These proxies may fail in detecting the consequences of increased nutrient loads on ben-thic systems (Dell’Anno et al. 2002) since they cannot provide any predictive information on the rate of organic matter inputs to the benthos (i.e. benthic trophic status; Jørgensen & Richardson 1996).
Benthic trophic status can be assessed in terms of total organic carbon (TOC) supply rate to the sea bot-tom (as g C m–2yr–1; Nixon 1995). However, this is dif-ficult to assess since the magnitude of the organic car-bon fluxes is not always directly linked to the primary production in the water column, and the assessment of all of the possible inputs of organic carbon is difficult to
© Inter-Research 2009 · www.int-res.com *Email: a.pusceddu@univpm.it
Quantity and bioavailability of sediment organic
matter as signatures of benthic trophic status
Antonio Pusceddu
1,*, Antonio Dell’Anno
1, Mauro Fabiano
2, Roberto Danovaro
11Department of Marine Sciences, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy 2Department for the Study of the Territory and its Resources, University of Genoa, Corso Europa, 26, 16100 Genova, Italy
ABSTRACT: Tools used for assessing marine trophic status are generally based on water column characteristics, which, however, may provide unreliable classification of the benthic trophic status. Here, we provide evidence from the literature that quantity and bioavailability of sediment organic matter are reliable proxies to assess benthic marine trophic status. We compiled data on the protein, carbohydrate and lipid concentration of sediments from different oceanic and coastal regions and varying water depths. The concentration of these 3 components as a whole (biopolymeric carbon) was found to be significantly correlated (r = 0.84) with the total organic carbon concentration, suggesting that the biopolymeric fraction is representative of the total organic carbon pool. However, the system-atic variation of the biopolymeric fraction was higher than that of total organic carbon concentrations, suggesting that biopolymeric carbon is a more sensitive proxy of benthic trophic status than is the total carbon pool. Furthermore, biopolymeric carbon was significantly correlated to the amount of phytopigments, indicating that biopolymeric carbon accumulation in the sediment is related to inputs of algal carbon. Biopolymeric carbon concentrations were also positively correlated to the sediment community oxygen consumption, suggesting that the progressive accumulation of biopolymeric car-bon could be an additional co-factor potentially responsible for hypoxic or anoxic events. The enzy-matically digestible and algal fractions of biopolymeric carbon decreased in sediments with increas-ing biopolymeric carbon content (i.e. eutrophic systems), suggestincreas-ing that organic carbon in eutrophic sediments is mostly refractory in nature. We propose that a biopolymeric carbon concentration in the sediment of > 2.5 mg C g–1, being associated with a bioavailable fraction of <10%, can be considered as a threshold level at which benthic consumers may experience mostly refractory organic carbon. KEY WORDS: Marine sediments · Organic matter · Trophic status
Mar Ecol Prog Ser 375: 41–52, 2009
achieve synoptically on large spatial and temporal scales (Lee et al. 1988). Another approach uses biolog-ical indicators such as presence and/or abundance of benthic diatoms and macroalgae (Duarte 1995, Kelly 1998), but the applicability of this method is limited to those systems characterised by the presence or domi-nance of living photosynthetic primary producers. Moreover, it does not provide any indication of the pos-sible consequences of eutrophication at higher trophic levels of the benthic food web. However, the conse-quences of changing trophic status reach all hierarchi-cal levels of the ecosystem organisation.
The response of consumers to increased organic matter supply is influenced more by organic matter quality (e.g. bioavailability) rather than by bulk con-centration in the ecosystem (Cebrián et al. 1998, Huxel 1999). Thus, the assessment of the trophic status needs to be extended to a more comprehensive description of the organic matter available for heterotrophic nutri-tion, and should include indicators of the quantity and bioavailability of all (including detrital) resources (Grall & Chauvaud 2002). This is particularly important for the assessment of the benthic trophic status, where the largest reservoir of food for benthic consumers is deposited (detrital) organic matter (Jørgensen & Richardson 1996).
Studies aiming at providing a reconstruction of long-term changes in the productivity of a given system have used stratigraphic analyses of organic carbon, nitrogen and phosphorus concentrations coupled with 210Pb geochronology (Cornwell et al. 1996), foramini-fera distributions (Duijnstee et al. 2004), and stable isotopic and lipid biomarker signatures in sediments (Zimmerman & Canuel 2002). These features allowed an assessment of historical changes in the trophic sta-tus of aquatic ecosystems only if analysed as a suite of indicators, since no indicator alone provided adequate information concerning the multiple, interrelated com-ponents of the ecosystems (Turner et al. 2006).
Alternatively, recent changes in the benthic trophic status through time can be detected by means of an analysis of organic carbon in superficial sediments. Several studies have provided evidence that eutrophi-cation is associated with a net accumulation or burial of organic carbon in the sediment (Cornwell et al. 1996, Emeis et al. 2000, Farías 2003). Other studies reported decreasing values of the C/N ratio in eutrophic sedi-ments (Sampou & Oviatt 1991).
Organic matter in marine sediments is composed of compounds exhibiting different levels of bioavailabil-ity for consumers, ranging from labile (i.e. immediately digestible, sensu Mayer et al. 1995) to refractory (recal-citrant to decomposition). Refractory compounds (such as humic and fulvic acids, structural carbohydrates and ‘black’ carbon) generally account for most of the
sedi-mentary organic matter, and due to very low degrada-tion rates, accumulate in marine sediments (Middel-burg et al. 1999). In contrast, highly labile compounds, representing the fraction of organic matter that is rapidly digested by benthic consumers, are subjected to greater temporal and spatial changes (Mayer et al. 1995). However, between these 2 opposite levels of bioavailability, there is a continuum of characteristics, which passes through intermediate levels of bioavail-ability. Unfortunately, the assessment of the lability of sediment organic carbon is not an easy task, and gen-erally implies several operational assumptions.
The biopolymeric fraction of sediment organic car-bon, measured as the sum of protein, carbohydrate and lipid carbon (BPC), has often been reported as the fraction of TOC potentially available to benthic con-sumers (Fabiano et al. 1995, Bianchelli et al. 2008). More recent investigations reported that only a frac-tion (5 to 30%) of these biopolymers is enzymatically digestible by consumers (Pusceddu et al. 2003).
In this work, we tested the following hypotheses: (1) BPC (sensu Fabiano et al. 1995) is related to TOC in marine sediments, (2) the algal fraction of BPC changes in sediments exhibiting different BPC concen-trations, (3) temporal variability in BPC concentration in the sediment changes under different benthic trophic status conditions, (4) sediment community oxy-gen consumption is related to BPC concentrations and (5) the enzymatically digestible fraction of BPC varies in sediments characterised by different trophic status.
Our goals were, thus, to (1) provide evidence that the quantity and bioavailability of BPC are reliable proxies for marine benthic trophic status, and (2) identify po-tential threshold levels of key organic carbon-related variables indicating trophic status shifts. To achieve these goals, we examined data from the published liter-ature for relationships between BPC and TOC concen-trations in marine sediments from different oceanic and coastal regions and water depths, including intertidal shallow waters and hadal depths. Then we explored the relationships between the quantity of BPC and (1) the algal carbon fraction associated with phytopig-ments, (2) the sediment community oxygen consump-tion (SCOC) and (3) the bioavailable (i.e. enzymatically digestible) fraction of sediment organic carbon (BAC).
MATERIALS AND METHODS
We compiled data published over the last 20 yr on phytopigment (chlorophyll a [chl a] and phaeopig-ment), protein, lipid, carbohydrate, BPC and TOC con-centrations in surface marine sediments worldwide (Table 1). Because of the multiple different sources of these data, we noticed that not all variables have been 42
Pusceddu et al.: Trophic status and sediment biochemistry
measured in all studies. All of the data used in this study were obtained from the scientific literature (see Table 1) using similar analytical methods. Possible biases due to different devices used for sediment sam-pling and/or the use of different analytical protocols were accurately checked (details are described later). Sediment samples (top 2 cm) were collected from coastal to hadal depths (i.e. from 0 to 7800 m water depth) using manual corers, Van Veen grabs, box-corers or multiple box-corers (Table 1). Previous studies have demonstrated that the quantity and biochemical compositions of sediment organic matter collected using multiple corers and box-corers display some dif-ferences (Shirayama & Fukushima 1995, Danovaro et al. 1998). However, since the differences in the con-centration of organic matter in sediments collected using different sampling devices are of the same order of magnitude as are the differences in organic matter concentrations determined on sediment replicates col-lected using the same sampling device (Danovaro et al. 1998), the data used in this study were not corrected. The concentrations of sedimentary chl aand phaeo-pigments were determined spectrophotometrically or spectrofluorometrically, according to standard proto-cols (Lorenzen & Jeffrey 1980). Total sedimentary lipids were extracted in chloroform:methanol (1:1, vol:vol; Bligh & Dyer 1959) and the resulting fraction, after evaporation in a dry hot bath at 80 to 100°C for 20 min, was quantified according to the sulfuric acid carbonisa-tion procedure (Marsh & Weinstein 1966). Data on total lipids presented in this study were expressed in tri-palmitine equivalents. The lipid fraction determined using this protocol allows the quantification of total lipid concentrations, but does not permit discriminating between different classes of lipids, which is different from chromatographic methods generally used in or-ganic geochemistry (Volkman 2006). However, this was not the main interest of the present study.
Total protein concentrations were determined ac-cording to Lowry et al. (1951) as modified by Hartree (1972) and Rice (1982) to compensate for phenol inter-ference and are expressed as bovine serum albumin (BSA) equivalents. Bradford’s (1976) protocol, used in some of the studies, provides results similar to Lowry et al.’s (1951) protocol (Berges et al. 1993) and, therefore, no corrections were applied. Total carbohydrate con-centrations, expressed in glucose equivalents, were obtained according to the Gerchacov & Hatcher (1972) protocol based on the phenol and concentrated sulfuric acid reaction with saccharides. The fractions of protein and carbohydrate enzymatically digestible were as-sessed according to Danovaro et al. (2001), modified for coastal sediments by Pusceddu et al. (2003), and reported as BSA and glucose equivalents, respectively. Briefly, enzymatically digestible proteins were
deter-mined as the difference between protein contents of intact sediments and sediments added with a solution of proteinase-K and protease after a 1 h incubation at 37°C. Protein analyses from these samples were car-ried out according to Lowry et al. (1951). Enzymatically digestible carbohydrates were determined as the dif-ference between carbohydrate quantities released by sediment added with a mixture of enzymes (α-amylase, β-glucosidase, proteinase-K, lipase) and by intact sedi-ments after 1 h incubation at room temperature. Carbohydrates from all supernatants and from intact sediments were analyzed according to Gerchacov & Hatcher (1972). Sediment subsamples muffled at 550°C for 4 h and processed as described previously were used as blanks. Concentrations of enzymatically digestible proteins and carbohydrates were normal-ized to sediment dry weight.
Total organic C concentrations in the sediment were determined according to Hedges & Stern (1984). BPC concentrations were calculated as the sum of protein, carbohydrate and lipid carbon equivalents, using con-version factors obtained from the elemental analysis of standard molecules (0.49, 0.4 and 0.75 µg C µg–1, respectively, for BSA, glucose and tripalmitine; Fabi-ano et al. 1995). Bioavailable carbon (BAC) concentra-tion was calculated as the sum of digestible proteins and carbohydrates converted into carbon equivalents by using the same factors as for their total pools (Danovaro et al. 2001). The algal carbon contribution to BPC was calculated as the percentage of chl a to BPC concentrations, after converting chl a concentration into carbon equivalents using a mean value of 40 µg C µg–1chl a (Pusceddu et al. 1999).
Statistical analyses. The relationships between the different fractions of sediment organic matter were assessed using either Type-I or Type-II regression analyses (Legendre & Legendre 1998). In particular, the Type-II regression analysis was carried out to avoid the underestimation of the slope of linear relationships between variables containing errors (Legendre & Legendre 1998). The Type-II regression analysis was carried out using the major axis regression method, since in all of the cases in the present study the vari-ables were expressed in the same physical units or were dimensionless (Jolicoeur 1990). Type-II regres-sion analyses were performed using the MODEL-II. exe routine (Legendre 2001).
The statistical differences between slopes and inter-cepts obtained from Type-I regressions testing for the relationships between variables in different environ-mental contexts were assessed by means of an analysis of covariance (ANCOVA). When slopes were found to be heterogeneous we used Tukey’s multiple compari-son tests (Zar 1984) to determine which combinations of ecosystems differed.
T
able 1. Mean value and range of pr
otein, carbohydrate, lipid, chl
a
and total or
ganic carbon (TOC) concentrations in marine sediments worldwide. DW = dr
y weight, na = not available, nd = not dete
rm ined Location Sampling Sampling Station Pr oteins Carbohydrates Lipids Chlor ophyll a T otal or ganic carbon Sour ce period device depth (mg g DW –1) (mg g DW –1) (mg g DW –1) (µg g DW –1) (mg g DW –1) (m) Mean Range Mean Range Mean Range Mean Range Mean Range Bar ents Sea na USNEL 0 – 500 6.0 5.2 – 6.7 0.4 0.3 – 0.5 nd nd 0.07 0.01 – 0 .14 n d n d
Pfannkuche & Thiel
spade cor er (1987) Bar ents Sea na USNEL spade cor er 501 – 1000 5.4 5.4 0.37 0.37 nd nd 0.06 0.06 nd nd “ Bar ents Sea na USNEL 1001 – 3920 3.4 2.1 – 4.7 0.30 0.26 – 0.35 nd nd 0.06 0.006 – 0.14 nd nd “ spade cor er Baltic Sea Sep 1981, Grab 18 na 3.8 – 7.7 nd 0.4 – 4.0 nd nd nd nd nd nd Meyer Reil (1983) Jun 1982
Baltic Sea (Kiel Bight)
Sep 1981, Grab na 7.1 6 – 8 2.3 0.7 – 3.4 nd nd nd nd nd nd
Meyer Reil & Graf (1986)
Apr 1982 Gulf of St. Lawr ence May – Jul 1988 Box-cor er 350 0.3 0.2 – 0.4 9.8 8.5 – 10.8 1.1 0.9 – 1.4 14.4 10.7 – 16.3 20.6 18.0 – 23.3 Colombo et al. (1996) NE Atlantic (Por cupine Sep 1996, Multicor er 4800 0.7 0.3 – 1.4 1.5 0.9 – 2.2 0.19 0.04 – 0 .78 n d n d n d n d Danovar o et al. (2001) Abyssal Plain) Mar 1997, Oct 1997 Gulf of Gascogne Fall 1984 Box-cor er 2100 1.9 na 2.4 na 0.2 na nd nd nd nd Khripounof f et al. (1985) Bar raña, Galicia Jan 1997, Manual Inter tidal 1.1 0.4 – 3.3 0.28 0.03 – 0.67 0.12 0.02 – 0 .31 n d n d 2.3 0.6 – 5.4 Cividanes et al. (2002) Jan 1998 cor er Gulf of Lions Oct 1983, Box-cor er 26 1.1 0.1 – 2.3 0.77 0.3 – 4.3 nd nd nd nd 4.8 2.4 – 7.3 Buscail et al. (1995) Dec 1985 Gulf of Fos Sep 1985, Manual 6 – 17 1.6 1.0 – 2.6 3.2 2.4 – 4.1 0.23 0.07 – 0 .66 1.9 0.4 – 5.9 11.1 6.9 – 15.8 Fichez (1991) Oct 1986 cor er
Ligurian Sea (Zoagli)
Feb 1990, Manual 10 0.03 0.02 – 0.07 0.3 0.13 – 0.67 0.1 0.02 – 0 .21 3.6 2.6 – 5.3 1.9 1.6 – 2.9 Fabiano et al. (1995) Feb 1993 cor er Ligurian Sea (Pr elo) Feb 1990, Manual 4 0.2 0.05 – 1.6 0.8 0.3 – 3.6 0.24 0.10 – 1 .08 0.7 0.1 – 1.8 3.4 1.7 – 16.1 Danovar o et al. (1994) Jan 1991 cor er Ligurian Sea Jul 1990 Grab 5 – 135 0.3 0.01 – 0.7 1.3 0.2 – 3.0 0.35 0.09 – 0 .88 2.3 0.6 – 7.1 nd nd Alber telli et al. (1999)
Ligurian Sea (Harbour)
Sep – O ct 1996 Manual 5 6.5 5.8 – 8.0 13.2 8.6 – 17.7 1.2 1.0 – 1.4 8.0 5.8 – 10.1 n d n d Danovar o et al. (1999c) cor er Ligurian Sea Jan 1991, Manual 4 0.1 0.02 – 0.3 0.9 0.3 – 5.3 0.23 0.09 – 0 .63 3.4 2.4 – 5.2 3.0 2.0 – 6.1 Danovar o & Fabiano Jan 1992 cor er (1997) Nor ther n Adriatic Sea Jun 1996, Manual 15 – 5 5 1.4 0.2 – 4.1 0.18 0.07 – 0.42 0.35 0.07 – 1.07 1.46 0.4 – 3.9 nd nd Danovar o et al. (2002) Feb 1997 cor er Nor ther n Adriatic Sea Jun 1996, Manual 15 – 5 5 1.8 0.9 – 3.7 0.22 0.09 – 0.64 0.33 0.14 – 0 .62 1.14 0.6 – 2.2 nd nd “ Feb 1997 cor er T y rr henian Sea Nov 1989 Grab 20 – 6 0 0.7 0.2 – 1.7 0.89 0.3 – 1.9 0.01 0.001 – 0.025 3.6 0.3 – 7.4 nd nd
Fabiano & Danovar
o (1994) T y rr henian Sea Jul 1997, Manual 10 2.4 1.6 – 3.3 1.3 0.5 – 2.8 1.06 0.3 – 2.1 nd nd nd nd Mazzola et al. (1999) Feb 1998 cor er T y rr henian Sea Jun 1993, Manual 0.5 – 2.5 6.0 2.2 – 12.1 12.8 0.8 – 70.5 1.6 0.3 – 4.5 4.6 0 – 77.6 nd nd Pusceddu et al. (1999) May 1994 cor er
Ionian and Aegean seas
Sep 1989 Box-cor er 0 – 500 0.12 0.11 – 0.15 1.8 1.6 – 2.3 0.12 0.09 – 0 .14 n d n d n d n d Danovar o et al. (1993)
Ionian and Aegean seas
Sep 1989 Box-cor er 501 – 1000 0.11 0.07 – 0.16 2.0 1.4 – 2.3 0.08 0.05 – 0 .16 n d n d n d n d “
Ionian and Aegean seas
Sep 1989 Box-cor er 1001 – 2401 0.11 0.07 – 0.13 1.9 1.2 – 2.5 0.10 0.05 – 0 .19 n d n d n d n d “ 44
Location Sampling Sampling Station Pr oteins Carbohydrates Lipids Chlor ophyll a T otal or ganic carbon Sour ce period device depth (mg g DW –1) (mg g DW –1) (mg g DW –1 ) (µg g DW –1 ) (mg g DW –1) (m) Mean Range Mean Range Mean Range Mean Range Mean Range Nor ther n Aegean Sea Mar – Apr 1997 Multicor er 0 – 500 2.2 0.4 – 3.5 3.9 1.2 – 5.9 0.47 0.3 – 0.8 3.8 1.0 – 7.9 nd nd Danovar o et al. (1999b) Nor ther n Aegean Sea Mar – Apr 1997 Multicor er 501 – 1000 4.0 1.8 – 6.6 5.0 3.6 – 6.5 0.67 0.5 – 0.8 4.2 0.3 – 10.1 nd nd “ Nor ther n Aegean Sea Mar – Apr 1997 Multicor er 1001 – 1271 4.7 4.5 – 5.0 6.9 6.4 – 7.3 1.2 1.1 – 1.3 3.3 1.0 – 5.7 nd nd “ Souther n Aegean Sea Aug – Sep 1997 Multicor er 500 – 1000 1.3 0.6 – 2.1 5.5 4.2 – 6.8 0.3 0.3 – 0.4 1.7 0.6 – 2.9 nd nd Danovar o et al. (1999b) Souther n Aegean Sea Aug – Sep 1997 Multicor er 1001 – 2270 1.6 0.5 – 3.5 6.2 1.0 – 11.6 0.33 0.1 – 0.7 3.8 0.2 – 1 1.4 n d n d “ Aegean Sea Sep 1989 Box-cor er na 0.2 0.1 – 0.2 2.4 1.7 – 3.0 0.09 0.02 – 0 .16 n d n d n d n d Danovar o et al. (1995) Cr etan Sea Sep 1995 Multicor er/ 40 – 500 0.6 0.5 – 0.7 1.0 0.6 – 1.5 0.25 0.11 – 0.35 1.1 0.1 – 2.6 nd nd Danovar o et al. (1998) box-cor er Cr etan Sea Sep 1995 Multicor er/ 501 – 1000 0.2 0.1 – 0.3 0.7 0.5 – 1.0 0.11 0.07 – 0.15 0.06 0 – 0.1 nd nd “ box-cor er Cr etan Sea Sep 1995 Multicor er/ 1001 – 1540 0.2 0.2 0.8 na 0.11 0.11 0.05 0.05 n d n d “ box-cor er Cr etan Sea Aug 1994, Multicor er 40 – 1540 1.0 0.2 – 3.0 1.9 0.2 – 7.9 0.17 0.03 – 0 .69 0 .54 < 0 .05 – 3.1 5.0 3.0 – 9.0 T selepides et al. (2000)
Mar 1995, May 1995, Sep 1995
Ionian Sea Jun 1993 Multicor er 500 – 1000 0.12 0.08 – 0.16 n d n d n d n d n d n d 5.5 5.2 – 5.8 Boetius et al. (1996) Ionian Sea Jun 1993 Multicor er 1001 – 4617 0.06 0.04 – 0.07 n d n d n d n d n d n d 4.6 4.1 – 5.3 “ Levantine Sea Jun 1993 Multicor er 0 – 500 0.06 0.06 n d n d n d n d n d n d 4.2 4.2 “ Levantine Sea Jun 1993 Multicor er 501 – 1000 0.09 0.09 n d n d n d n d n d n d 6.2 6.2 “ Mactan, Philippines na na na na 0.5 – 1.3 na 0.7 – 1.6 nd nd nd nd nd nd
Graf & Meyer Reil (1985)
Demerara Abyssal Plain
Sep 1981 Box-cor er 4440 2.4 na 1.8 na 0.3 na nd nd nd nd Sibuet (1984) Atlantic Ocean Sep 1981 Box-cor er 4850 1.9 na 1.7 na 0.3 na nd nd nd nd “ South Pacific Sep 1997 Box-cor er 1061 – 1355 3.4 1.6 – 6.2 1.9 0.7 – 4.3 1.0 0.6 – 1.9 6.1 2.8 – 1 1.8 n d n d Danovar o et al. (2003) (Atacama T rench) South Pacific Sep 1997 Piston 7800 2.6 2.6 0.3 na 0.6 0.6 2.0 2.0 nd nd Danovar o et al. (2003) (Atacama T rench) cor er
Ross Sea (Antar
ctica) Jan – Feb 1995 Grab 37 – 223 1.9 1.0 – 4.9 5.4 2.2 – 13.3 0.22 0.12 – 0 .40 1 0.2 1.9 – 2 7.8 n d n d Pusceddu et al. (2000) Mediter ranean May 1995 – M anual 2 4.8 0.2 – 8.5 6.5 0.1 – 12.0 0.9 0.1 – 1.5 4.1 0.5 – 2 0.0 n d n d Pusceddu et al. (2003) coastal lagoon Feb 1996 cor er Souther n Adriatic Mar – Sep 2000 Grab/ 10 – 5 0 1.5 01 – 14.0 3.7 0.1 – 12.2 0.3 0.04 – 2.4 13.3 1.2 – 43.5 n d n d Dell’Anno et al. (2002)
and Ionian seas
multicor er Alicante, Spain Sep 2003 Manual 27 – 3 0 2.0 1.8 – 2.3 8.3 6.1 – 12.7 0.5 0.3 – 0.7 11.3 6.5 – 1 8.5 7.0 5.8 – 9.3
Pusceddu et al. (2007a)
(fish far m sediments) Pachino, Italy Sep 2002 Manual 30 1.1 0.4 – 2.0 4.3 1.9 – 6.6 0.2 0.1 – 0.4 1.6 0.8 – 2.5 3.8 1.2 – 5.0 “ (fish far m sediments) Sounio, Gr eece Jul 2003 Manual 20 – 2 5 0.9 0.6 – 1.2 4.8 0.5 – 11.2 0.5 0.3 – 0.7 0.5 0.1 – 0.8 4.3 0.0 – 8.3 “ (fish far m sediments) Cypr us Jul 2002 Manual 30 – 3 5 3.0 1.5 – 5.3 3.8 1.9 – 5.4 0.7 0.4 – 1.1 2.8 2.0 – 2.4 5.3 3.0 – 8.3 “ (fish far m sediments)
Ross Sea (Antar
ctica) Nov 1994, Box-cor er 439 – 567 2.1 0.2 – 3.4 0.59 0.4 – 0.8 0.21 0.01 – 0.38 0.3 0.2 – 0.4 nd nd
Fabiano & Danovar
o (1998)
Jan 1995
T
able 1 (continued)
Mar Ecol Prog Ser 375: 41–52, 2009
Systematic variations in BPC and TOC concentra-tions and temporal variability in concentration of BPC in different ecosystems were assessed as the value of mean squares after a 1-way ANOVA was performed using sampling time as a single source of variance, separately for each data set.
PRIMARY PRODUCTION AND SEDIMENT ORGANIC ENRICHMENT
Relatively few studies have reported synoptic deter-minations of TOC and BPC concentrations. Using a reduced data set available from a few studies carried out in the Mediterranean Sea, we found that BPC is significantly related to TOC (Fig. 1). The BPC repre-sents 71% of the TOC variance, while the remaining 29% is ascribed to other factors such as the variable composition and importance of the refractory fractions (Middelburg et al. 1999). However, whilst the biopoly-meric fraction undergoes rapid changes in quantity and composition during early diagenesis, TOC gener-ally exhibits a more conservative nature (Fabiano et al. 1995). This suggests that changes in the quantity of BPC might respond to changes and/or differences in the systems’ productivity more promptly than TOC.
To test this hypothesis, we examined the relationship between proxies of primary production and BPC. The input of primary organic matter to the sea bottom (together with the benthic algal biomass, if present) is generally assessed using phytopigment concentrations in surface sediments (Pfannkuche et al. 2000). In our analysis, the total phytopigment concentrations (the sum of chl a and phaeopigments, expressed as carbon equivalents) explained only about 13% of BPC vari-ance (Type-I regression: r2= 0.127, n = 124, p < 0.01), with the remaining 87% being ascribed to other sources, including non-marine sources, of organic mat-ter enmat-tering the system. Since photosynthetic pigments are labile compounds (Lee et al. 2000), their concentra-tion in surface sediments may reflect primary produc-tion processes only at shallow water depths. In con-trast, their progressive depletion during particle sinking through the water column will generally re-sult in a progressive decrease of the
phytopigment concentration in deep-sea sediments in moving from bathyal to abyssal depths (Fabiano et al. 2001). The weak relationship that we observed between phytopigment con-centrations and BPC concentration is, therefore, potentially biased by the data collected at deeper depths. The analysis of different types of coastal ecosystems, in fact, indicates a much
closer relationship between total phytopigment and BPC concentrations (Fig. 2a), with significant changes seen in the slope of the linear regressions (Table 2). Despite the fact that the 3 selected areas represent only part of the primary production levels found world-wide, the observed pattern suggests that the BPC in oligotrophic coastal systems (e.g. Ligurian Sea) is more closely dependent upon the input of primary organic matter than that in eutrophic systems (e.g. Adriatic Sea).
We observed decreasing algal carbon contributions to the BPC pools with increasing BPC concentrations in the sediment (Fig. 2b). The comparison of environ-ments characterised by diverse organic matter input and different productivities indicates that increasing accumulation of BPC in marine sediments is associated even in highly productive systems (such as estuaries, ponds and fish farm sediments) with low algal carbon contributions to BPC. This suggests that, in eutrophic sediments characterised by high BPC concentrations and benthic algal biomass, algal carbon is progres-sively diluted in a complex and heterogeneous organic matrix. In this regard, however, it must be considered that the carbon:chl a ratio of living algae can vary from 10 to about 100 (Banse 1977). Since we used a ratio of 46 R2 = 0.71 0 3 6 9 12 15 0 2 4 6 8 10 Biopolymeric C (mgC g–1) Total organic C (mg C g
–1) Thermaikos Gulf (eutrophic)
Ligurian Sea (oligotrophic) Cretan Sea (oligotrophic)
Fig. 1. Type-I (continuous line) and Type-II (dashed line) lin-ear regressions between TOC and BPC concentrations in Mediterranean sediments. Data are extracted from Fabiano et al. (1995) for Ligurian Sea, Tselepides et al. (2000) for Cretan Sea and Pusceddu et al. (2005) for Thermaikos Gulf. R2is the
coefficient of Type-I regression
Table 2. Output of the analysis of covariance (ANCOVA) testing for differences between slopes and intercepts of Type-I regressions illustrated in Fig. 2a.
***p < 0.001, *p < 0.05, ns = not significant, na = not applicable F Multiple comparisons ANCOVA comparison Slope Intercept Slope Intercept Liguran Sea (L) vs Ross Sea (R) 32.20*** 0.37 ns L > R na Ross Sea (R) vs Adriatic Sea (A) 4.21* 5.86* R > A R < A Ligurian Sea (L) vs Adriatic Sea (A) 4.04* 0.006 ns L > A na
Pusceddu et al.: Trophic status and sediment biochemistry
40, our estimates of the algal carbon contribution to BPC are potentially biased by a factor of up to 2 to 4. Moreover, we compared systems characterised by a wide variability in depositional regimes, so that the values of the algal carbon contribution to BPC should be considered with some caution.
Sediments exhibiting different BPC loads are also characterised by different temporal variability pat-terns. Marine sediments characterised by high BPC loads, such as coastal lagoons and organically enriched sediments beneath cages at fish farms, display a more pronounced temporal variability. Conversely, benthic systems characterised by lower BPC contents are char-acterised by a much lower temporal variability (Fig. 3). This result suggests that under ‘eutrophic’ conditions (i.e. high primary productivity) the inputs of organic carbon widely fluctuate, determining strong and
sud-den shifts of background levels of sediment organic matter concentrations. Conversely, in oligotrophic sys-tems, the seasonal organic carbon input during algal blooms does not detectably alter background concen-trations of organic matter in the sediment.
BIOPOLYMERIC CARBON AND OXYGEN DEMAND Organic matter reaching the sediment surface stimu-lates benthic metabolism (Witbaard et al. 2001). This has been used for carrying out a worldwide estimate of particulate organic carbon fluxes to the deep ocean (>1000 m in depth) from benthic oxygen flux estimates (Jahnke 1996). In turn, the accumulation of organic carbon in the sediment is also a function of organic car-bon reactivity with the available oxygen (Dauwe et al. 47 0 20 40 60 80 100 Biopolymeric C (mg C g–1)
Algal carbon contribution (%)
Harbour Pond Hadal depocenter Coastal oligotrophic Deep oligotrophic Estuary Fishfarm biodeposits
b
0 1 2 3 4 5 6 7 8 9 Phytopigments (mg C g–1) Biopolymeric C (mg C g –1) Ligurian Sea (Oligotrophic) y = 7.25x + 0.001 Ross Sea (Mesotrophic) y = 1.40x + 0.72 Adriatic Sea (Eutrophic) y = 0.58x + 0.57a
4 5 6 7 0 1 2 3 8 9 0 2 4 6 8 10Fig. 2. Type-II regressions between phytopigment (chl a and phaeopigment in C equivalents) and BPC concentrations in marine sediments in 3 coastal ecosystems with (a) different primary productivity levels, and (b) relationship between the fraction of BPC that is made up by phytopigments (= algal carbon contribution, expressed as the percentage of chl a carbon equivalents) and BPC concentrations in marine sediments. Data for (a) are extracted from Fabiano et al. (1995) for Ligurian Sea, Pusceddu et al. (2000) for Ross Sea and Danovaro et al. (2002) for Adriatic Sea. In (b), grey circles represent the mean values of representative sediments
Mar Ecol Prog Ser 375: 41–52, 2009
2001). When the sediment experiences an excessive organic input, oxygen can be completely depleted, with anaerobic processes prevailing.
We have found significant relationships between in
situ measurements of SCOC and synoptic
measure-ments of TOC and BPC concentration of the sediment (Fig. 4). The results of Type-I regression indicated that concentrations of both pools explained significant proportions of the variance of oxygen consumption rates, but whilst total organic carbon explained 61% of SCOC variance, BPC alone can explain 79% of SCOC variance. From the linear equations calculated using Type-II regression, it can be calculated that an in-crease of 1 mol C m–2in sediment BPC concentration would enhance SCOC by about 100 µmol m–2 h–1, which is about 2-fold higher than the SCOC increase obtained by an equal increase in TOC concentration
(about 53 µmol m–2h–1). These results indicate that the BPC is more labile towards degradation than is the total carbon pool and suggest that an enrichment in the BPC concentration, more than in TOC, will shift the system towards conditions of higher oxygen demand. The ecological consequences of excessive organic accumulation in the sediment will also depend upon the hydrodynamic regime and other environmental constraints (e.g. water mixing, temperature, salinity, pressure, biological activity), to which the remaining 21 to 39% of the unexplained variance in the relation-ships outlined previously can be ascribed. Nonethe-less, our results suggest that high BPC concentrations in surface sediments might be an additional co-factor potentially responsible for the development of hypoxic and/or anoxic events (Dell’Anno et al. 2008).
BIOPOLYMERIC AND BIOAVAILABLE ORGANIC CARBON RELATIONSHIPS: TROPHIC
CONSEQUENCES
Since BPC may contain molecules that become avail-able to consumers only after microbial reworking, the use of BPC as a proxy for labile organic carbon depends also on its origin and molecular composition. The amount of labile (bioavailable) organic matter in marine sediments can be extrapolated according to 48 0.0 5.0 10.0 15.0 20.0 25.0 30.0 0.0 5.0 10.0 15.0 20.0 Temporal variance (MS) Eutrophic Lesina lagoon n = 3 Eutrophic Goro lagoon n = 4
a
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 0.0 1.0 2.0 3.0 4.0 Biopolymeric C (mg C g–1) Te mporal variance (MS) Eutrophic Fish-farm sediments n = 6 Eutrophic Gulf of Thermaikos n = 3 Mesotrophic N Adriatic Sea n = 6 Oligotrophic Seagrass sediments n = 15 Oligotrophic Abyssal N Atlantic n = 4 Oligotrophic Ligurian Sea n = 36b
Fig. 3. Relationship between BPC sediment content and its temporal variability in different marine environments. Tem-poral variability is reported as mean squares (MS) derived af-ter a 1-way ANOVA performed using sampling time as a sin-gle source of variance, separately for each data set; (b) is an enlarged view of the inset in (a). Horizontal bars indicate SE values. Data plotted refer to Manini et al. (2003) for coastal la-goons, Mazzola et al. (1999) for fish farm sediments, Pusceddu et al. (2005) for Thermaikos Gulf, Danovaro et al. (2002) for N Adriatic Sea), Danovaro et al. (1994) for seagrass sediments, Fabiano et al. (1995) for Ligurian Sea, and Danovaro et al.
2001 for Atlantic sediments y = 52.5x
0 500 1000 1500 2000 0 5 10 15 20 0 5 10 15 20 Organic C (mol C m–2) SCOC (µmol m –2 h –1) SCOC (µmol m –2 h –1)
a
y = 100.5x 0 500 1000 1500 2000 Biopolymeric C (mol C m–2) Harbour sediments Hadal N Atlantic Mediterranean Seab
Fig. 4. Relationships between sediment community oxygen consumption (SCOC) and (a) total organic carbon and (b) BPC concentrations in the sediment. Data are summarised from Danovaro et al. (1999a, 2002), Witbaard et al. (2000), Duineveld et al. (2000), Tselepides et al. (2000) and Lykousis et al. (2002).
Pusceddu et al.: Trophic status and sediment biochemistry
mathematical models based on the exponential de-crease of organic carbon with increasing depth in the sediments (Rice & Rhoads 1989). Such models, how-ever, assume that different classes of organic com-pounds undergo degradation and utilisation at similar rates (Danovaro et al. 2001).
A number of studies demonstrated that only a certain fraction of BPC in marine sediments can actually be degraded enzymatically and, thus, is readily available for heterotrophic nutrition (Dauwe & Middelburg 1998, Dauwe et al. 1999a,b, Dell’Anno et al. 2000, Danovaro et al. 2001). Based on this background, we investigated the relationship between concentrations of BPC and bioavailable carbon (BAC) in sediments characterised by different productivity levels (Fig. 5a). As expected from the linear relationship between BPC and the sediment community oxygen consumption, BAC is positively correlated with BPC, suggesting that
eutro-phic (i.e. enriched in BPC concentration) sediments are characterised also by high concentrations of rapidly digestible material. However, increasing BPC concen-trations in the sediment also display a progressive de-crease of the percentage contribution of the bioavail-able carbon to BPC (Fig. 5b). This finding would indicate that benthic environments subjected to changes in trophic status may experience relevant changes in the relative importance of the labile and refractory fractions of sediment organic carbon. These changes could be also the result of differences in sedi-ment particle characteristics, which are known to play a major role in the preservation (and, thus, lability) of the different pools of sediment organic matter (Keil et al. 1994). Nevertheless, our results are in agreement with previous studies indicating that eutrophic sys-tems, subjected to the accumulation of large amounts of organic matter in subsurface sediments, could be 49 0 10 20 30 40 50 60 70 80 Biopolymeric C (mg C g–1) B ioavai la bl e C (% of B P C ) Unvegetated oligotrophic Seagrass sediments Trawled sediments Untrawled
sediments Eutrophicated lagoons
Abyssal sediments
b
y = 0.055x + 0.02 0.0 0.5 1.0 1.5 2.0 2.5 3.0 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35 B io a v a ila b le C (m g C g –1)a
Fig. 5. Relationships between (a) BPC and BAC quantities and (b) the bioavailable (enzymatically digestible) fraction of BPC versus BPC quantity in marine sediments. Data are extracted from Danovaro et al. (2001) for the Porcupine Abyssal Plain (4850 m depth), Pusceddu et al. (2003) for the western Mediterranean Sea (2 m depth), Pusceddu et al. (2005) for the eastern Mediter-ranean Sea (30 to 86 m depth) and Pusceddu et al. (2007b) for the Goro and Lesina lagoons. The light grey area encloses values of BPC concentrations less than 2.5 mg C g–1, which correspond to values of the bioavailable fraction >10%. The equation
Mar Ecol Prog Ser 375: 41–52, 2009
characterised by an enhancement of the complexation of buried organic molecules with the inorganic matrix, thus making them less ‘available’ to heterotrophic nutrition (the so-called ‘sorptive preservation hypothe-sis’; Mayer 1994). This could be also due to an ‘en-capsulation’ mechanism of potentially labile molecules (such as proteins) in organically enriched sediments (such as those buried in the sapropel layers; Knicker & Hatcher 1997). The accumulation of mostly refractory organic matter in organically enriched sediments appears to be the case of transitional (lagoonal) eco-systems (e.g. Pusceddu et al. 2003).
From these relationships, it can also be seen that when BPC concentrations in the sediment exceed 2.5 mg C g–1, its bioavailable fraction is always less than 10%. These 2 values, when verified contempo-rarily in the same area, can, thus, be proposed as threshold levels out of which accumulation of BPC leads to altered organic matter bioavailability to ben-thic consumers.
Acknowledgements. This study was undertaken in the frame-work of the PR1 project funded by the Italian Ministry of the Environment, and with NITIDA (COFIN2003) funding pro-vided by the Italian Ministry of University and Research. We are grateful to G. Sarà, S. Fraschetti and M. A. Colangelo for help in statistical analyses and 4 anonymous reviewers who gave constructive comments on early versions of the manuscript.
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Editorial responsibility: Matthias Seaman, Oldendorf/Luhe, Germany
Submitted: June 20, 2007; Accepted: September 12, 2008 Proofs received from author(s): January 15, 2009
